© 2002 by The Society for Integrative and Comparative Biology
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The Geography of Evolutionary Opportunity: Hypothesis and Two Cases in Gastropods1
1 Department of Geology, University of California at Davis, One Shields Avenue, Davis, California 95616
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Evolutionary innovations that require or provide increased per-capita energy budgets and competitive performance should appear at times and in places where resources are abundant and accessible and where predators and competitors impose intense selection. By contrast, innovations without functional benefits should become established in productive environments under conditions of weak selection from enemies. I confirmed these predictions in comparative studies of two types of innovation in gastropod shells. The labral tooth, a structure facilitating predation, appeared in 45 Cenozoic clades of marine gastropods, with the highest concentrations originating during the early Miocene, late Miocene, and Pliocene, all times and sites of high planktonic productivity, large expanses of warm shallow water, and diverse predator-rich biotas. Left-handed coiling, a condition with no obvious survival benefits, arose 19 times independently in right-handed clades. Most left-handed clades, including eight arising in regions outside the tropics, evolved in productive regions where the larva and/or the adult is shielded from intense predation. The times and places of origin of new traits in clades thus offer insights into the geography of evolutionary opportunity.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONHYPOTHESISTHE LABRAL TOOTH IN...LEFT-HANDED GASTROPODSCONCLUSIONSReferences Cited |
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Read almost any taxonomic monograph, and you will encounter the obligatory section on biogeography. Typically it is an interesting account of the geographic distribution of species, clades, or the somewhat more abstract notion of taxonomic diversity; but at its core, it remains a geography of names. For me, biogeography has always meant more than that. In my travels, I have been captivated not only by the intersection of species distributions and regional history, by clades spreading and contracting as barriers come and go, and by the dramatic contrasts in diversity between rich equatorial and impoverished high-latitude sites, but also by the geography of characteristics. Quite apart from differences in species richness, regions vary interestingly in the range of phenotypes and in the degree of expression or specialization of adaptive characteristics. It isn't just the names or the numbers of species that change; it is the conditions of life these species encounter and accommodate that vary from place to place and over time. There is a geography of context—the physical, chemical, and biological environments in which evolution takes place.
In this paper I want to concentrate on what I call the geography of evolutionary opportunity. By evolutionary opportunity I mean the circumstances permitting or favoring the origin and spread of innovations, phenotypic traits that newly appear in a clade. I outline a general hypothesis for the geographic origin of evolutionary innovations, and illustrate the expected patterns with a comparative study of two contrasting types of innovation in gastropod shells: an adaptive type, exemplified by the labral tooth, and a type without apparent survival function, the transition from right-handed to left-handed coiling. I argue that evolutionary opportunity is concentrated in places and at times of large, warm, productive ecosystems and biotas, and that adaptive innovations originate and become established under conditions of intense selection by enemies. Left-handedness and other survival-neutral novelties also require productive (or at least permissive) environments, but thrive best in situations where animals are shielded from enemies.
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HYPOTHESIS |
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Nearly all evolutionary innovations that improve their bearers' competitive, defensive, and reproductive performance are energetically costly. This is so whether the innovation arises as a developmental modification in ontogeny, or as a symbiosis between evolutionarily unrelated partners. Any novelty, even one that provides a potential advantage, must in some sense compete with established adaptations. It does not originate fully formed or fully functional, and is therefore not likely to be immediately superior to other older designs. Improvement is therefore most likely in a permissive environment, one characterized by what can be described as general economic growth. In the human arena, such major innovations as agriculture, steam engines, and advances in the manufacture of textiles and weapons took place in growing economies in which productive capacity was high (Lewis, 1955
; McNeill, 1982; Mokyr, 1990). Similarly in nonhuman economies, a surplus of biologically accessible energy and raw materials may be a precondition for the origin and establishment of energy-intensive, adaptive innovations. Innovation may itself enhance the surplus and increase the productivity of the unit in which it occurs and in the environment of that unit because of positive feedback—positive returns, in the language of economists—between innovations and resources (Mokyr, 1990, 1991; Vermeij, 1995).
Novelties are improvements only if they function effectively in the competitive context of other organisms. Any trait that increases its bearer's power—its rate of performing work—potentially confers such an advantage provided that its bearer exists in an environment where energy and material resources are both available and "easy" (energetically inexpensive) to acquire. In other words, an evolutionary innovation that enables its bearer to become more productive, to move faster, to apply greater force, to accomplish a task in less time, to sense opportunities and dangers at greater distances, or to grow faster, requires a surplus of resources—in short, a growing economy. The most potent innovations will arise in those growing economies where the intensity of competition in the broad sense (including predation) is already high, for it is in these settings that the bar of performance is set very high (Vermeij, 1987, 1995, 1999).
On the geographic scale, conditions like this are satisfied in regions with three characteristics: large habitat size (area or volume), warm conditions, and abundant raw materials where they can be taken up from water or soil by primary producers. A large habitat area permits small populations of scattered individuals to persist without the threat of stochastic extinction. The high metabolic rates that are associated with energy-intensive, power-enhancing adaptations are also associated with small population sizes. This is the case, for example, with top predators among endothermic birds and mammals, and with ecologically dominant large trees (Bakker, 1980; Vermeij, 1987; Burness et al., 2001). Fast-growing weeds, too, depend on large effective habitats for their long-term maintenance. Their fast growth, powered by rapid metabolism or photosynthesis, takes advantage of briefly favorable circumstances arising from disturbances. Success in such disturbed areas is contingent on rapid response, but it is short-lived, for competitively superior species typically take over. This means that weeds are subject to wide fluctuations in population size. Weeds are unlikely to persist as populations in the long run if the habitat they collectively occupy is small, because they are subject to stochastic extinction. Large habitats therefore can support species that, in various contrasting ways, evolve power-enhancing, energy-intensive adaptations and physiologies. Small environments, on the other hand, constrain the metabolic rates and therefore the competitive power of species confined to them.
This scenario explains the observation, first clearly articulated by Darwin (1859), that large habitats—those on continents and in large ocean basins—are more likely to evolve weedy species and competitive dominants than are smaller island-like habitats. High growth rates, high metabolic rates, and large numbers of offspring characterize continental species or those widely distributed in coastal oceanic waters, but are rare or absent on islands. Importantly, therefore, islands differ from larger land or water masses not only in their lower diversity and in their comparative isolation, but also in their potential for spawning high-powered species with high levels of short-term and long-term competitive, defensive, and reproductive performance.
Warm conditions similarly are highly favorable to the evolution of high performance. At least up to a temperature of about 40°C, many functions—rates of biochemical reaction, locomotion, feeding, photosynthesis, growth, and nerve transport—increase as temperature rises (Gillooly et al., 2001; Vermeij, 2002). Moreover, functions dependent on viscosity, such as filter-feeding and swimming, become energetically less expensive in warmer water. The same is true for the precipitation of calcium carbonate in skeletons (see Vermeij, 2002, for a review). Higher temperatures therefore make many processes cheaper, and make available pathways of adaptation that would be out of adaptive reach as being too costly in the cold (see also Vermeij, 1978, 1987).
Finally, the high metabolic rates that are prerequisites for high levels of economic performance can be sustained only if material resources are available and accessible. Soils must be fertile, with the minerals not bound into refractory compounds; and waters must be rich in dissolved nutrients, oxygen, and plankton. These conditions are satisfied in areas of active chemical weathering, such as mountainous and volcanic regions, and lands drained by flooding rivers, and in coastal waters characterized by upwelling, river and estuarine inputs or nutrients, or dust-laden winds. Coastal waters adjacent to large, topographically complex land masses are thus much more productive than are waters in parts of the open ocean far from land or waters surrounding small islands.
If large, warm, productive habitats preferentially harbor organisms and ecosystems with the highest economic performance, these geographic regions should also emerge as the loci of origin of evolutionary novelties that have retrospectively proved to allow their bearers to hold their own against entrenched incumbents. However, it is one thing to have the high metabolic rate that provides the potential to compete successfully with incumbents, but quite another to realize that potential. For example, having a high growth rate as most weeds do does not guarantee competitive success against shade-casting, large, late-succession trees. Innovations have great potential, but they do not start as well-crafted adaptations. For the most part, they will be found wanting when faced with the well-tested traits of highly adapted incumbents. A prerequisite for realizing the potential is therefore the convenient elimination or disabling of incumbents. This can occur when some catastrophe strikes, a catastrophe to which competitive dominants are more vulnerable than are disturbance-dependent weeds. In the absence of highly adapted incumbents, the weeds have the potential to evolve more sophisticated long-term competitive mechanisms as they take the place of their antecedents.
I thus identify two types of disturbance that are important in the origin and spread of energy-intensive evolutionary innovations with a high competitive potential. One type of disturbance is brief and local; it favors the evolution of short-lived, fast-growing, prolific weeds that can capitalize on favorable conditions of short duration. The second type is more severe, occurring on a spatial and temporal scale great enough to eliminate competitive dominants. In the post-crisis scramble, weeds take advantage of their rapid growth and high fecundity to colonize vacated environments and thus to be the first that become established. Subsequently, given sufficient resources, they have the potential, with their inherited high metabolic rates, to evolve a wide range of adaptations that confer high performance in competition, defense, and reproduction.
This scenario for the origin and spread of adaptive innovations and for competitively dominant lineages has been supported in a general way by studies on major innovations. Fast-growing weedy angiosperms, for example, evidently originated in productive lowland environments in the tropics, and displaced well-entrenched gymnosperms and other plants in other environments as crises ravaged these incumbents (Wing and Boucher, 1998). Using taxonomic rank as a proxy for major evolutionary innovations, Jablonski (1993) showed that most such innovations during the last 250 million years arose in the tropics. Generally fast-growing bivalved molluscs originated in near-shore environments, and later joined slower growing brachiopods offshore. During the later Mesozoic, when productivity may generally have risen in nearshore marine environments, bivalves restricted brachiopods increasingly to unproductive, cold, oxygen-starved marine settings (Vermeij, 1987; Droser and Sheehan, 1997). There is an essentially similar story among bryozoans. Energy-intensive cheilostome bryozoans arose nearshore in the Late Jurassic, and diversified and ecologically expanded at the expense of slower-growing, less fecund cyclostomes (McKinney, 1995).
Most studies of innovation, including those mentioned above, account for the earliest appearance of a given novelty, but not for later independent origins of similar innovations in the same or other clades. Moreover, biologists tend to analyze evolutionary innovations only in extant groups. For example, powered flight among vertebrates is known in only two living clades, the birds and the bats. The fossil record, however, shows that it originated in a third clade, the pterosaurs, and did so earlier (in the Late Triassic) than in the other two (Late Jurassic and perhaps early Cenozoic for birds and bats respectively). Data from fossil groups are thus essential to the evaluation of ideas about the origin and spread of evolutionary innovations. Ideally, all instances of origin of a given type of innovation should be included.
Testing these ideas is difficult and rarely done. The most suitable innovations for tests of the hypothesis of evolutionary opportunity satisfy four criteria: (1) they must be directly observable in living and fossil material; (2) the clades in which the innovations occur must be prolifically represented in the fossil record; (3) the clades must be phylogenetically sufficiently known that a place and time of origin of the innovation in question can reasonably be inferred from phylogenetic and stratigraphic evidence; and (4) the innovation must be sufficiently minor that it evolved repeatedly in several clades, so that patterns of spatial and temporal origin can be analyzed statistically against null hypotheses based on sampling effort, collecting bias, and other problems associated with fossil data.
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THE LABRAL TOOTH IN GASTROPODS |
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SYNOPSISINTRODUCTIONHYPOTHESISTHE LABRAL TOOTH IN...LEFT-HANDED GASTROPODSCONCLUSIONSReferences Cited |
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In a previous study (Vermeij, 2001
), I evaluated the geographic and evolutionary opportunity of innovation by analyzing the times and places of first appearance of a minor adaptive innovation in the shells of predatory gastropods. The innovation in question is the labral tooth, a tooth-like or spine-like protrusion pointing toward the substratum on the edge of the outer (abaxial) lip of the aperture. Where it has been studied functionally, the tooth has been shown to increase the rate of predation on hard-shelled prey such as barnacles and bivalves. It may have additional benefits in predation, but these remain speculative. The labral tooth forms at different points along the lip, is either a permanent fixture throughout growth or a discontinuously produced structure formed during interruptions in spiral growth, and represents the extension of an external spiral cord, a spiral groove, or of a larger sector of the lip as a whole. Phylogenetic, stratigraphic, and other evidence indicates that the tooth has evolved at least 58 times independently in marine tonnoidean and neogastropod clades, beginning about 80 Ma during the Campanian stage of the late Cretaceous (Vermeij, 2001). Half the known cases occur in the single neogastropod family Muricidae. These numbers may increase slightly as more refined data become available, but overall patterns are unlikely to change. All tooth-bearing clades appear first in warm-temperate or tropical regions, and in these regions tooth-bearing species comprise a higher proportion of the larger clades to which they belong than do tooth-bearing species in colder climates. Among the 45 post-Eocene clades, 30 (67%) appeared and likely originated in one of the four major tropical regions: 11 in the Indo-West Pacific, eight in the western Atlantic, five in the eastern Pacific, and six in the eastern Atlantic (including the subtropical Neogene Mediterranean). The other 15 clades are known first in warm-temperate regions: three each in the northeastern Pacific, New Zealand, and western South America; two each in the northwestern Pacific and southern Africa; and one each in the northwestern and northeastern Atlantic. Only about four percent of the 251 living tooth-bearing species occur in cool-temperate waters, but all belong to clades with a warm-water origin. There are no polar tooth-bearers. Suitable cold-water faunas in which tooth-bearing clades could have appeared are known from the Neogene of the North Pacific, New Zealand, and southern South America.
First appearances of clades with a labral tooth cluster in the late Cretaceous (nine clades), early Miocene (12 clades), late Miocene (six clades), and Pliocene (7 clades) (Fig. 1). There are no clades appearing in the early Paleocene or early Oligocene, intervals following significant episodes of extinction. The pattern of temporal appearance of clades with a labral tooth differs significantly from that expected on the basis of the number of available fossiliferous formations and the number of formations with exceptionally rich faunas (400 species or more) (Vermeij, 2001). Intervals when first appearances of tooth-bearing gastropods exceed null expectations are characterized by high planktonic productivity (as inferred from the large size of suspension-feeding bivalves, barnacles, and gastropods) and by a wide latitudinal extent of tropical and subtropical conditions. The long Eocene epoch witnessed only four independent first appearances of gastropods with a labral tooth. Suspension-feeders in most of the world during the Eocene were small compared to those of the Miocene to Recent interval, perhaps indicating that planktonic productivity was relatively low in the inshore habitats where tooth-bearing gastropods would have lived. Warm conditions were latitudinally more extensive in the Eocene than during any subsequent interval, but the only large-bodied molluscs in the very rich faunas of the European and American Eocene were herbivores and predators.
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The data on gastropods with a labral tooth therefore largely conform to expectations derived from the hypothesis of evolutionary opportunity. Adaptive, energy-intensive innovations arise preferentially in warm, productive environments.
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LEFT-HANDED GASTROPODS |
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It is instructive to compare the pattern of origins of an adaptive innovation such as the labral tooth with the pattern of first appearances of an innovation that is unlikely to have significant survival-related benefits. A trait of the latter type is left-handedness (or sinistrality) in shell coiling. Left-handedness arises as a complete reversal of shell and body asymmetry from a right-handed (dextral) condition, which typifies the great majority of gastropods. In a right-handed shell, the aperture appears on the observer's right when the shell is held with the apex up and the aperture facing the observer. Handedness is known to affect patterns of mating in gastropods (Lipton and Murray, 1979
; Gittenberger, 1988; Asami, 1993), making it likely that the establishment of sinistrality in dextral lineages is associated with sexual selection. Sinistral individuals in normally dextral populations often deviate slightly in shell form from wild-type dextrals (Gould et al., 1985; Vermeij, 1993), perhaps implying that the left-handed condition has small deleterious side effects. There is no evidence that handedness affects survival after hatching.
Although sinistral individuals are known in many normally dextral species (Rolán-Alvarez and Rolán, 1995), left-handedness as a characteristic of species is rare in most gastropod clades. Sinistrality at the species level is very common in land and freshwater pulmonates (Vermeij, 1975; Asami, 1993; Pierce, 1996; Palmer, 1996), but I have found it in only 19 post-Cretaceous clades of marine gastropods. The fossil record of nonmarine gastropods and of pre-Cenozoic marine gastropods is inadequate for reliable estimation of times of appearance of reversed coiling. I therefore limit myself to Cenozoic marine gastropods.
My current tally indicates that left-handedness at and above the species level arose 19 times independently among Cenozoic marine gastropods (Table 1). Most left-handed clades (13, 68%) belong to the Neogastropoda. I suggest that left-handedness arose twice in the buccinid genus Neptunea, once in the northeastern Atlantic during the early Pliocene (N. contraria clade) and once in the biogeographically isolated Okhotsk Sea perhaps during the Pleistocene (N. leva). The two species belong to different lineages within Neptunea (Goryachev, 1987); the N. contraria lineage appears to be derived from the N. lyrata clade when the latter invaded the Atlantic from the Pacific during the Pliocene (Strauch, 1972), whereas N. leva appears to be derived from N. rugosa, a member of the N. polycostata clade (Golikov et al., 1987). I suggest that left-handedness arose three times in borsoniine turrids, once each in the West African Asthenotoma sinistralis, the Brazilian Borsonia brasiliana, and the late Eocene southeastern American Sinistrella americana. Gofas (1990) had suggested that A. sinistralis and T. americana are congeneric, implying that the two species might belong to the same lineage; but the extremely rich fossil record of the Miocene and Pliocene in the eastern and western Atlantic lacks sinistral representatives of this group, and differences in the columella between A. sinistralis and S. americana indicate that left-handedness evolved independently in these two taxa.
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The temporal distribution of first appearances of sinistral clades as documented by fossils generally differs from that of clades with a labral tooth (Fig. 1). First appearances were spread out in time except for the Pliocene, when there was a concentration of five first appearances of sinistral clades. In two cases, the time of origin of left-handedness is likely to be earlier than is indicated by earliest appearance. Two clades for which only living sinistral species are known (Sinistralia in the northwestern Indian Ocean and northwest Africa, and Blauneria in the Caribbean and Indo-West Pacific) probably originated during or before the early Pliocene, when land barriers that now separate the regions these clades inhabit last became established. Blauneria may have an Oligocene or even earlier origin in Europe given its close similarity to Stolidotoma, a genus with a stratigraphic range from the Paleocene to the Oligocene (Martins, 1996
). Three left-handed clades (Pakistania, Kallosinistrala, and Antistrepsus) are either stratigraphically isolated or occur in regions with a poor and discontinuous record. Their times of first appearance are therefore not well constrained. I have taken the origin of the sinistral Triphoridae to be early Paleocene following the careful study of this group by Nützel (1998). The geographic distribution of sinistral Cenozoic marine clades also contrasts with that of tooth-bearing clades. Left-handedness has appeared in at least three exclusively cold-temperate to polar clades during the Neogene (Antistreptus in the southern hemisphere, and Neptunea leva and Pyrulofusus in the Northwestern Pacific), and in at least five clades from mild-temperate regions ("Calliostoma" incertum in southern Australia, Kallosinistrala in the Antarctic Peninsula, Antiplanes in the northwestern Pacific, and the Neptunea contraria and "Terebra" inversa clades in the northeastern Atlantic). All these temperate clades originated in highly productive regions, and all originated at higher latitudes and in cooler waters than did the 15 Neogene temperate tooth-bearing clades. Among 14 post-Eocene sinistral clades, seven (50%) are restricted to, and likely originated in, tropical to subtropical seas: three in the Western Atlantic (Sinistrofulgur and Contraconus in the southeastern United States and Borsonia brasiliana in Brazil), two in West Africa (Asthenotoma sinistralis in Senegal, Scaevatula in the Gulf of Guinea), and two in unknown areas but possibly also in the eastern Atlantic (Sinistralia and Blauneria). With the possible exception of Borsonia, these tropical to subtropical clades occupy and evolved in highly productive environments.
Many productive regions did not produce sinistral clades. This is strikingly the case in the Miocene to Recent continental Indo-West Pacific, tropical and warm-temperate eastern Pacific, and continental Caribbean. Sinistral clades also did not originate in the less planktonically productive insular Indo-West Pacific and Caribbean. These regions, especially the post-Miocene Indo-West Pacific, are characterized by intense predation-related selection in shallow-water ecosystems. Molluscan shell armor, locomotor defense, and specialized host-guest symbioses reach their peak of expression in the tropical Indo-West Pacific, and diminish from the tropics to the poles (Vermeij, 1978, 1989, 1993). I interpret this geographic pattern to mean that predators and other biotic sources select against the minor morphological side effects of sinistrality.
Further evidence that species-level sinistrality originated in environments where predator-induced selection is weak comes from the biology of living left-handed species. All sinistral neogastropods and the pulmonate Blauneria have a nonpelagic larval stage. Sinistrality, which is expressed in the unfertilized egg, therefore develops in the comparative safety of a capsule or egg mass. Adult Blauneria live in sediment beneath mangrove leaf litter (Martins, 1996), where predation by larger animals is likely to be rare. Two sinistral clades (Triphoridae and Laiocochlis) live on or in sponges (Nützel, 1998). The habits of "Calliostoma" incertum have not been described, but almost all calliostomatid trochoideans are associated with nematocyst-bearing cnidarian hosts (Marshall, 1995), which like sponges offer protection against many types of predator.
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Two case studies are obviously insufficient for a thorough test of the hypothesis of evolutionary opportunity, but they point the way to many similar analyses that could be undertaken with minor innovations in many other kinds of organisms. Innovations in the structure or number or arrangement of leaves, bones, teeth, clonal parts, appendages, shells, and sense organs are all amenable to studies of the type illustrated here.
Both types of innovation I have considered—the functional, performance-enhancing labral tooth and the apparently functionless reversal in shell coiling from right-handedness to left-handedness—are most likely to arise when resources are abundant and accessible. Strong selection by enemies favors innovations that increase power. By the same token, such selection is inimical to the evolution of traits like sinistrality that at least in their early stages of development are accompanied by mildly deleterious side effects. Resources provide opportunities for phenotypes to deviate from established norms; intense selection from biotic sources under conditions of affluence favors those deviations that require a high investment in energy and that enhance fitness. Innovations that reduce absolute costs and that do not lead to a larger power budget should predominate in settings where resources are scarce or where access to those resources is severely constrained by such factors as intense competition and predation, low temperatures, low oxygen concentrations, and environments in which movement is restricted by clutter. The fossil record offers a rich source of data for further exploring these links between geography and evolutionary innovation.
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FOOTNOTES |
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1 From the Symposium Integrated Approaches to Biogeography: Patterns and Processes on Land and in the Sea presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: vermeij{at}geology.ucdavis.edu
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